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Effects of temperature on Paramoeba perurans growth in culture and the associated microbial community

Published online by Cambridge University Press:  25 October 2018

O. Benedicenti*
Affiliation:
Scottish Fish Immunology Research Centre, Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK Marine Scotland Science Marine Laboratory, 375 Victoria Rd, Aberdeen AB11 9DB, UK
C. J. Secombes
Affiliation:
Scottish Fish Immunology Research Centre, Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
C. Collins*
Affiliation:
Marine Scotland Science Marine Laboratory, 375 Victoria Rd, Aberdeen AB11 9DB, UK
*
Author for correspondence: O. Benedicenti, E-mail: ottavia.benedicenti@gmail.com and C. Collins, E-mail: Catherine.Collins@gov.scot
Author for correspondence: O. Benedicenti, E-mail: ottavia.benedicenti@gmail.com and C. Collins, E-mail: Catherine.Collins@gov.scot

Abstract

Population growth, in vitro, of three Paramoeba perurans cultures, one polyclonal (G) and two clonal (B8, CE6, derived from G), previously shown to differ in virulence (B8 > G > CE6), was compared at 10 and 15 °C. B8 showed a significantly higher increase in attached and in suspended amoebae over time at 15 and 10 °C, respectively. CE6 and G also had significantly higher numbers of suspended amoebae at 10 °C compared with 15 °C at experiment termination. However, in contrast to B8, numbers of attached amoebae were significantly higher at 10 °C in CE6 but showed a similar trend in G at the end of the experiment. Numbers of both suspended and attached amoebae were lower in B8 compared with CE6 and G. Significant differences in bacterial community composition and/or relative abundances were found, between cultures, between temperatures and between the same culture with and without amoebae, based on 16S rRNA Illumina MiSeq sequencing. Bacterial diversity was lower in B8 and CE6 compared with G, possibly reflecting selection during clonal isolation. The results indicate that polyclonal P. perurans populations may contain amoebae displaying different growth dynamics. Further studies are required to determine if these differences are linked to differences seen in the bacterial communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Adams, MB and Nowak, BF (2003) Amoebic gill disease: sequential pathology in cultured Atlantic salmon, Salmo salar L. Journal of Fish Diseases 26, 601614.Google Scholar
Bovee, EC and Sawyer, TK (1979) Marine flora and fauna of the Northeastern United States. Protozoa: Sarcodina: Amoebae. NOAA Technical Report, National Marine Fisheries Service Circular 419, 156.Google Scholar
Bowman, JP and Nowak, B (2004) Salmonid gill bacteria and their relationship to amoebic gill disease. Journal of Fish Diseases 27, 483492.Google Scholar
Bridle, AR, Crosbie, PBB, Cadoret, K and Nowak, BF (2010) Rapid detection and quantification of Neoparamoeba perurans in the marine environment. Aquaculture 309, 5661.Google Scholar
Bridle, AR, Davenport, DL, Crosbie, PBB, Polinski, M and Nowak, BF (2015) Neoparamoeba perurans loses virulence during clonal culture. International Journal for Parasitology 45, 575578.Google Scholar
Burgess, SL and Petri, WA (2016) The intestinal bacterial microbiome and E. histolytica infection. Current Tropical Medicine Reports 3, 7174.Google Scholar
Bustos, PA, Young, ND, Rozas, MA, Bohle, HM, Ildefonso, RS, Morrison, RN and Nowak, BF (2011) Amoebic gill disease (AGD) in Atlantic salmon (Salmo salar) farmed in Chile. Aquaculture 310, 281288.Google Scholar
Clark, A and Nowak, BF (1999) Field investigations of amoebic gill disease in Atlantic salmon, Salmo salar L., in Tasmania. Journal of Fish Diseases 22, 433443.Google Scholar
Collins, C, Hall, M, Bruno, D, Sokolowska, J, Duncan, L, Yuecel, R, McCarthy, U, Fordyce, MJ, Pert, CC, McIntosh, R and MacKay, Z (2017) Generation of Paramoeba perurans clonal cultures using flow cytometry and confirmation of virulence. Journal of Fish Diseases 40, 351365.Google Scholar
Crawley, MJ. (2007). The R Book, 1st Edn. Chichester, West Sussex, UK: Wiley.Google Scholar
Crosbie, PBB, Bridle, AR, Cadoret, K and Nowak, BF (2012) In vitro cultured Neoparamoeba perurans causes amoebic gill disease in Atlantic salmon and fulfils Koch's postulates. International Journal for Parasitology 42, 511515.Google Scholar
Douglas-Helders, M, Saksida, S, Raverty, S and Nowak, BF (2001) Temperature as a risk factor for outbreaks of amoebic gill disease in farmed Atlantic salmon (Salmo salar). Bulletin of the European Association of Fish Pathologists 21, 114116.Google Scholar
Douglas-Helders, GM, O'Brien, DP, McCorkell, BE, Zilberg, D, Gross, A, Carson, J and Nowak, BF (2003) Temporal and spatial distribution of paramoebae in the water column – a pilot study. Journal of Fish Diseases 26, 231240.Google Scholar
Douglas-Helders, M, Nowak, B and Butler, R (2005) The effect of environmental factors on the distribution of Neoparamoeba pemaquidensis in Tasmania. Journal of Fish Diseases 28, 583592.Google Scholar
Downes, JK, Henshilwood, K, Collins, EM, Ryan, A, O'Connor, I, Rodger, HD, MacCarthy, E and Ruane, NM (2015) A longitudinal study of amoebic gill disease on a marine Atlantic salmon farm utilising a real-time PCR assay for the detection of Neoparamoeba perurans. Aquaculture Environment Interactions 7, 239251.Google Scholar
Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 24602461.Google Scholar
Edgar, RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996998.Google Scholar
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C and Knight, R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 21942200.Google Scholar
Embar-Gopinath, S, Butler, R and Nowak, B (2005) Influence of salmonid gill bacteria on development and severity of amoebic gill disease. Diseases of Aquatic Organisms 67, 5560.Google Scholar
Embar-Gopinath, S, Crosbie, P and Nowak, BF (2006) Concentration effects of Winogradskyella sp. on the incidence and severity of amoebic gill disease. Diseases of Aquatic Organisms 73, 4347.Google Scholar
Embar-Gopinath, S, Bowman, J, Carson, J, Crosbie, P and Nowak, B (2008) A culture-dependent 16S rRNA gene-based approach to identify gill bacteria associated with amoebic gill disease in Atlantic salmon. Bulletin of the European Association of Fish Pathologists 28, 2734.Google Scholar
Francés, R, Benlloch, S, Zapater, P, González, JM, Lozano, B, Muñoz, C, Pascual, S, Casellas, JA, Uceda, F, Palazón, JM, Carnicer, F, Pérez-Mateo, M and Such, J (2004) A sequential study of serum bacterial DNA in patients with advanced cirrhosis and ascites. Hepatology 39, 484491.Google Scholar
Fringuelli, E, Gordon, AW, Rodger, H, Welsh, MD and Graham, DA (2012) Detection of Neoparamoeba perurans by duplex quantitative taqman real-time PCR in formalin-fixed, paraffin-embedded Atlantic salmonid gill tissues. Journal of Fish Diseases 35, 711724.Google Scholar
Handl, S, Dowd, SE, Garcia-Mazcorro, JF, Steiner, JM and Suchodolski, JS (2011) Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse faecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiology Ecology 76, 301310.Google Scholar
Ihaka, R and Gentleman, R (1996) R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5, 299314.Google Scholar
Jellett, JF and Scheibling, RE (1988) Effect of temperature and prey availability on growth of Paramoeba invadens in monoxenic culture. Applied and Environmental Microbiology 54, 18481854.Google Scholar
Lozupone, C, Lladser, ME, Knights, D, Stombaugh, J and Knight, R (2011) Unifrac: an effective distance metric for microbial community comparison. ISME Journal 5, 169172.Google Scholar
McCarthy, U, Hall, M, Schrittwieser, M, Ho, YM, Collins, C, Feehan, L, Simons, J and White, P (2015) Assessment of the viability of Neoparamoeba perurans following exposure to hydrogen peroxide. A study commissioned by the Scottish Aquaculture Research Forum (SARF). Available at http://www.sarf.org.uk/.Google Scholar
McMurdie, PJ and Holmes, S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, 111.Google Scholar
Mouton, A, Crosbie, P, Cadoret, K and Nowak, B (2013) First record of amoebic gill disease caused by Neoparamoeba perurans in South Africa. Journal of Fish Diseases 37, 407409.Google Scholar
Munday, BL, Foster, CK, Roubal, FR and Lester, RJG (1990) Paramoebic gill infection and associated pathology of Atlantic salmon, Salmo salar, and rainbow trout, Salmo gairdneri, in Tasmania. In Perkins, FO and Cheng, TC (eds), Pathology in Marine Science. London, UK: Academic Press, pp. 215222.Google Scholar
Paniagua, E, Parama, A, Iglesias, R, Sanmartin, ML and Leiro, J (2001) Effects of bacteria on the growth of an amoeba infecting the gills of turbot. Diseases of Aquatic Organisms 45, 7376.Google Scholar
Steinum, T, Kvellestad, A, Rønneberg, LB, Nilsen, H, Asheim, A, Fjell, K, Nygård, SMR, Olsen, AB and Dale, OB (2008) First cases of amoebic gill disease (AGD) in Norwegian seawater farmed Atlantic salmon, Salmo salar L., and phylogeny of the causative amoeba using 18S cDNA sequences. Journal of Fish Diseases 31, 205214.Google Scholar
Wang, Q, Garrity, GM, Tiedje, JM and Cole, JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 52615267.Google Scholar
Young, ND, Dyková, I, Nowak, BF and Morrison, RN (2008) Development of a diagnostic PCR to detect Neoparamoeba perurans, agent of amoebic gill disease. Journal of Fish Diseases 31, 285295.Google Scholar
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